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103 Journal of Exercise Physiologyonline June 2013 Volume 16 Number 3 JEPonline EOdffiitcoira-li nR-eCsheieafr ch Journal of Totmhem Ay mBoeorincea,n P ShoDc, iMetByA o f ReEvixeewrc Bisoea rPdh ysiologists Todd Astorino, PhD Heart Rate Variability (HRV) as a Tool for Diagnostic Julien BIaSkSeNr ,1 P09h7D- 9751 Steve Brock, Ph D and Monitoring Performance in Sport and Physical Lance Dalleck, PhD Activities Eric Goulet, PhD Robert Gotshall, PhD Alexander Hutchison, PhD Bojan Makivić¹, Marina Djordjević Nikić2, Monte S. Willis3 M. Knight-Maloney, PhD Len Kravitz, PhD 1Center for Sport Science and University Sport, University of Vienna, James Laskin, PhD Auf der Schmelz 6, 1150 Vienna, Austria, 2Faculty of Sport and Yit Aun Lim, PhD Lonnie Lowery, PhD Physical Education, University of Belgrade, Blagoja Parovića 156, Derek Marks, PhD 11000 Belgrade, Serbia, 3McAllister Heart Institute, University of North Cristine Mermier, PhD Carolina, 2336 Medical Biomolecular Research Building, Campus Box Robert Robergs, PhD # 7525, NC 27599 Chapel Hill, USA Chantal Vella, PhD Dale Wagner, PhD Frank Wyatt, PhD ABSTRACT Ben Zhou, PhD Makivić B, Djordjević Nikić M, Willis MS. Heart Rate Variability (HRV) as a Tool for Diagnostic and Monitoring Performance in Sport and Physical Activities. JEPonline 2013;16(3):103-131. The dynamic autonomic responses during exercise can be measured to give Official Research Journal actionable information for training by analysis of the ECG to determine of the American Society of heart rate variability (HRV). While application of HRV has been Exercise Physiologists applied to predict sudden cardiac death and diabetic neuropathy in assessing disease progression, recent studies have suggested that it ISSN 1097-9751 may be applied to exercise training. In this review, we present the rationale for measuring HRV. We describe the different variables used and what they can tell us about the autonomic nervous system. The use of HRV in detecting changes in exercise intensity is presented, along with evidence that gender and age changes may affect autonomic HRV. Lastly, we illustrate how HRV measurements taken immediately post-exercise have proven to be useful in measuring and monitoring training load to proscribe workouts and/or prevent over- training. Despite the studies that vary widely in their application to different training levels of athletes being tested and HRV measures used, the standardization of methodologies and results should help accelerate the use of HRV in sports training. Key Words: Autonomic Nervous System; Overtraining; HRV 104 TABLE OF CONTENTS ABSTRACT------------------------------------------------------------------------------------------------------------ 103 1. INTRODUCTION ------------------------------------------------------------------------------------------------- 105 1.1 ORIGINS OF HEART RATE VARIABILITY (HRV) MEASUREMENTS------------------ 105 1.2 BASICS OF THE AUTONOMIC NERVOUS SYSTEM AND ITS REGULATION OF HRV ------------------------------------------------------------------------------------------------- 105 1.3 COMMONLY USED HRV PARAMETERS/DESCRIPTORS ------------------------------ 107 1.4 APPLICATION OF HRV ON EXERCISE ------------------------------------------------------- 108 1.5 EXPERIMENTAL APPROACH TO THE PROBLEM ---------------------------------------- 109 2. RESULTS ---------------------------------------------------------------------------------------------------------- 109 2.1 BASICS OF HEART RATE VARIABILITY (HRV)-----------------------------------------------110 2.2 MEASUREMENT OF HRV DURING DIFFERENT EXERCISE INTENSITIES --------110 3. ASSOCIATION OF EXERCISE, GENDER, AND AGE WITH AUTONOMIC TONE ------------113 4. HRV MEASUREMENT TAKEN POST-EXERCISE: WHAT THEY CAN TELL US ABOUT EXERCISE JUST COMPLETED ----------------------------------------------------------------------------- 114 4.1 HRV TAKEN IMMEDIATELY POST-EXERCISE DURING RECOVERY REFLECTS THE EFFECTS OF THE EXERCISE ON THE BODY --------------------------------------- 114 4.2 EXERCISE LOAD DISTRIBUTIONS ARE REFLECTED BY HRV POST-EXERCISE114 4.3 TRAINED ATHLETES HAVE DIFFERENT HRV POST-EXERCISE THAN LESS TRAINED ATHLETES ------------------------------------------------------------------------------- 114 4.4 HIGH FREQUENCY POWER (HFP) (VAGAL REACTIVATION) AFTER EXERCISE IS BLUNTED WITH EXERCISE INCREASED EXERCISE INTENSITY IN SEDENTARY WOMEN ------------------------------------------------------------------------------115 4.5 POST-EXERCISE, LFP, AND TP ARE INCREASED WITH INCREASE WORKLOAD IN MALE ENDURANCE ATHLETES -------------------------------------------------------------115 5. HRV AS A MONITORING TOOL IN ATHLETIC TRAINING PROGRAMS------------------------- 118 6. HRV, OVERTRAINING, AND OVER-REACHING STATES ------------------------------------------- 121 7. DISCUSSION ------------------------------------------------------------------------------------------------------ 125 8. SUMMARY---------------------------------------------------------------------------------------------------------- 126 9. REFERENCES------------------------------------------------------------------------------------------------ 127 105 1. INTRODUCTION The way in which the cardiovascular system responds to the stress of exercise has captured the imagination of sports physiologists for the past century (5). Critical adjustments are continually made to the cardiovascular system to meet the diverse demands of the musculature and heart (16,51). These dynamic adjustments in cardiac and peripheral vascular control, including their regulation by the autonomic nervous system (ANS), occur in response to rapid changes in heart rate and blood pressure. Analysis of electrocardiographic (ECG) tracings allows for the measurement of the autonomic nervous system. The application of heart rate variability (HRV) to assess risk for sudden cardiac death and diabetic neuropathy is well known (28,44). However, the use of HRV in monitoring sports training is in its infancy, despite technological advances in heart rate monitors that allow the collection of ECG tracings fairly conveniently. In this review, we present the underlying rationale for HRV measurement as a surrogate marker of autonomic nervous system function, the commonly used analytics applied to HRV, and present how HRV has been applied to exercise in athletes and non- athletes alike. We then review the literature to illustrate how HRV measures change with different exercise intensities, and describe how exercise, gender, and age changes may affect the autonomic tone determined by HRV. Lastly, we describe the utility of taking HRV measurements immediately post-exercise to determine training load and present how HRV may be used as a monitoring tool in athletic training programs to avoid over-training. Despite studies that vary widely in their application to different training levels of the athletes being tested and HRV measures used, standardization of methodologies and the publishing of results are still needed and will help accelerate the potential use of HRV monitoring in sports training in the future. 1.1 Origins of Heart Rate Variability (HRV) Measurements In 1733, Stephen Hales first observed variation in arterial pressure and beat-to-beat time length during the respiratory cycle in horses (8,9). The first documented report of variability of and cardiac rhythms is credited to Carl Ludwig in 1847, when he documented respiratory sinus arrhythmia (RSA) using a smoked drum kymograph, a device he invented that allowed for the measurement of mechanical activity (8,9). Using galvanometers in the early 20th century, William Einthoven produced the first continuous recordings of the electrical activity of the heart (8,9). In early 1960s, Norman Jeff Holter developed a small portable device capable of obtaining long-term ambulatory ECGs (>24 hr) (9). The device resulted in exponential growth in information regarding the relationship between HRV and disease. Time domain analysis was performed on these early ECG measurements, whereas frequency domain analysis did not exist until the early 1970s (9). The detection of heart rate variability in relation to monitoring performance in physical activities is a relatively new field that detects changes in the autonomic system in response to exercise. 1.2 Basics of the Autonomic Nervous System and Its Regulation of HRV The sympathetic and parasympathetic (autonomic) nervous systems innervate the heart and regulate heart rate (HR). The balance between these systems affects the consistency in the time between heart beats; a measure determined by calculated the heart rate variability (HRV). As illustrated in Figure 1 the HRV represents a physiological phenomenon that may be monitored and analyzed to determine the state of the nervous system that controls the heart. A simple method of detecting the autonomic response involves determining variations in consecutive time intervals between peaks of the QRS complex called the R-R interval, which can be collected in relatively simple devices such as modern wrist computers (1,37,50). 106 Figure 1. Model of HRV Control. This illustrates independent actions of the vagal, α- and β- sympathetic system. Their action can be assessed by measuring heart rate variability, blood pressure variability, and the baroreflex mechanism. The parasympathetic nervous system is responsible for the bradycardia accompanying baroreceptor stimulation, and for the tachycardia accompanying baroreceptor deactivation, with the sympathetic nervous system also playing a minor role (5). The effects of the ANS on the heart’s R-R intervals are complex, resulting from both innervation of the heart and the vasculature. The heart and circulatory system are controlled primarily by higher brain centers (central command) and cardiovascular control areas in the brain stem through the activity of the ANS, which is composed of sympathetic and parasympathetic nerves. The medulla is the primary site to regulate sympathetic and parasympathetic (vagal) outflow to the heart and blood vessels. Specifically, the nucleus tractus solitarius in the medulla receives sensory input and stimulates cardiovascular responses to emotion and stress, including physical stress (e.g., exercise). From the medulla, the parasympathetic vagus nerve innervates the heart, as do sympathetic nerve fibers. The right and left vagus nerves innervate the sinoatrial (SA) and atrioventricular (AV) nodes, respectively. The atria are also innervated by vagal efferents, whereas the ventricular myocardium is sparsely innervated by vagal efferents. Sympathetic efferent nerves are present throughout the atria (including the conduction system), particularly in the SA node and ventricles. Sympathetic stimulation increases the heart rate, contractility, and conduction velocity, whereas parasympathetic stimulation has the opposite effect. Sympathetic effects are mediated through adrenoreceptors (alpha and beta). Parasympathetic effects are relayed through muscarinic receptors. Autonomic control of the cardiovascular system is also affected by baroreceptors, chemoreceptors, muscle afferents, local tissue metabolism, and circulating hormones (5) (Figure 2). Although both the sympathetic and parasympathetic systems are active at rest, the parasympathetic fibers release acetylcholine, which acts to slow the pacemaker potential of the SA node and thus reduce heart rate. 107 Figure 2. R-R Variations of R-R Distance, Measured Above, Make Up the Data Used to Calculate the Heart Rate Variability (HRV). Adapted from Aubert et al. (5). 1.3 Commonly Used HRV Parameters/Descriptors The most commonly used HRV parameters in ANS evaluation are the frequency-domain, time- domain, and Poincaré plot parameters. While the nomenclature of the different measurements is complex, they represent different ways to look at the variability and distribution of the heart rate over time and parallel the similar, and unique, uses of mean, median, and mode as descriptors of population measurements. Frequency-domain analysis describes high and low frequency rates of the variability changes, which correspond to the activity of different branches of the ANS. By applying these frequency range differences in HRV analysis, researchers are able to distinguish the individual contributions of the sympathetic and parasympathetic systems (1,2). Low-frequency (LF) modulation (0.04-0.15 Hz) of R-R interval changes corresponds to the sympathetic and parasympathetic activities together. High-frequency (HF) modulation (0.15-0.4 Hz) of R-R interval changes is primarily regulated through innervation of the heart through the parasympathetic (vagal) nerve. In the second HRV parameter described here, common time-domain parameters reflect the standard deviation (SD) of all N-N intervals (SDNN) that reflect the total variability and the root mean square of SDs between adjacent N-N intervals (RMSSD), which reflects parasympathetic activity (1). The N-N interval here corresponds to the R-R interval of normal (sinus) beats. In the third HRV parameter represented by the Poincaré plot, a person’s R-R intervals are plotted over time and standard deviation is used to interpret changes seen in the plot. The standard descriptor 1 (SD1) represents the fast beat-to-beat variability in the R-R intervals, while the standard descriptor 2 (SD2) describes the longer-term variability (47). The SD1 reflects mainly the parasympathetic input to the heart, while SD2 reflects both sympathetic and parasympathetic contributions to the heart. The HRV increases when respiratory frequency decreases. Although respiration greatly affects the HRV, the absence of standardized models of respiratory frequency makes it difficult to interpret HRV 108 data from that perspective. According to the previous studies, researchers have accepted various respiratory frequency ranges (e.g., from 6 to 15 breaths·min-1). However, it is clear that a self- organized respiratory pattern should be maintained during the recording period (15,42,43,49). Also, it is important that standard protocols and methods for research with athletes should be established with regard to exercise intensity and duration, respiration rate, position of the body during recording, and duration of recording (5). 1.4 Application of HRV on Exercise Based on data from major indexing sources, the number of studies that have examined heart rate variability (HRV) in general has steadily increased at least 5-fold since 1990 (through 2012), and the number investigating the influences of different physical activities on HRV has risen dramatically since 1999 (Figure 3). The HRV has long been investigated for its role in cardiac health during disease processes. However, recent studies have shown that HRV parameters change during and after exercise. These findings suggest that the HRV parameters could be used to analyze the stress the body experiences during training and to gain insight into physiological recovery after training. In fact, it is reasonable that changes in the autonomic nervous system (ANS) patterns reflected by changes in the HRV may serve as useful parameters for managing physical fatigue and exercise intensity (3). Moreover, information regarding the extent to which the body recovers after training may provide useful data for the personalization of sports training, training loads, and recovery times. Figure 3. The Number of Publications Having the Key Words “Heart Rate Variability” (HRV), HRV and Sport, Overtraining, and Physical Training has Continued to Increase Since 1990. Based on searches made on four major biomedical and sports medicine databases (detailed in 1.5 Experimental Approach to the Problem Section). 109 In this review, we summarize how HRV analysis has been reported in sport science. We also discuss the advantages and limitations of the applications of these studies to the training and monitoring of the physiological performance of athletes. 1.5 Experimental Approach to the Problem Four major biomedical and sports medicine databases (PubMed, MEDLINE, NSCA, and ACSM) were reviewed for studies on heart rate variability and it relationship to exercise training from 1990-2011. The 2001-2010 Proceedings of the German Union for Sport Science were also reviewed. The Union holds annual conferences to discuss the application of HRV in sports. The key search terms were: heart rate variability, HRV and sport, HRV and overtraining, HRV and physical activity, and HRV and physical fatigue. Given the diversity of athlete populations studied, the methodologies and training regimens used, and the mathematical analyses applied in these studies, meta-analysis was not possible. Subjects and Procedures. To be included in this review, studies had to incorporate research and athletes, individuals who exercised regularly, or sedentary individuals challenged with exercise. Also, the studies had to include the Institutional Review Board or Ethics Committee approval of their projects including the appropriate informed consent. 2. RESULTS Most athletes understand the importance of recovery after exercise, which is defined as the return of body homeostasis after training to pre-training or near pre-training levels. Recovery involves getting adequate rest before training continues to allow the body to repair and strengthen itself between workouts. By allowing recovery to pre-training or near pre-training levels, recovery supports optimizing future performance. However, according to Zatsiorsky and Karaemer (52) this near-training level is based on the constantly changing dynamic of the athlete and the amount of further training that is encountered. Recovery seeks to minimize the negative effects of training, such as fatigue, of the previous workout while retaining the positive effect (i.e., physical fitness and improved performance). To optimize recovery, monitoring after workouts is very important to avoid excessive accumulation of physical fatigue during preparation or competition. If recovery is not achieved, performance begins to decline, as is seen in the overtraining syndrome in which training for an event or the event itself pushes beyond the body’s ability to recover. Researchers in the field of sport science are intensely engaged in identifying tools to estimate the quantity of physical stress in the training process needed to optimize competitive performance. The goal of training is to put a sufficient training load on the body to disturb homeostasis and the whole autonomic balance. Athletes may expect a better response in terms of physiological adaptation only if the recovery of the body is sufficient (24). The question then becomes how to measure the recovery level in an objective manner to maximize the benefits of training. Traditionally, researchers studying recovery and performance level in the experimental laboratory have assessed aerobic fitness by measuring various parameters, including the maximum oxygen uptake (VO max), minimum velocity needed to reach VO max (vVO max), velocity at the onset of 2 2 2 blood lactate accumulation (VOBLA), and repeated sprint abilities. Other factors in the blood have also been described, including creatine kinase, cortisol, white blood cell counts, C-reactive protein (CRP), myeloperoxidase protein levels (MPO), and glutathione status (17,27). Although these measures are periodically used to determine performance and recovery (12,38), they are either too expensive or complicated for everyday use, even for professional athletes. In addition to requiring large, expensive equipment that is found primarily in performance laboratories, exercise physiologists 110 must be available to conduct the tests and analyze the results. Accordingly, scientists and coaches are looking for useful, noninvasive methods to obtain valuable data about physiological changes that occur in response to physical activity. Optimal training depends on matching the specific abilities of the individual, such as muscle strength, endurance, explosiveness, and flexibility to the individual’s aerobic capacity, training load, and recovery. Since improvements and adjustments in each of these abilities are constantly changing with continued training, balancing these multiple components to prevent overtraining can be challenging. To this end, the use of heart rate variability (HRV) may be one logical solution because it reflects the major regulatory processes after exercise. While multiple recent studies have used HRV to detect which measures change in relationship to exercise type and intensity, its use also illustrates how monitoring physical fitness during exercise and the post-exercise periods may be applied to athletic training more broadly in the future (11,21). 2.1 Basics of Heart Rate Variability (HRV) The lengths of successive R peaks (RR) in the QRS complex can be described mathematically; the R-R parameter is not consistent between successive R peaks. How this measure varies can be described mathematically in a number of different ways. During the onset of physical activity, R-R intervals become shorter and more uniform (less varied), resulting from increased sympathetic activity and parasympathetic withdraw. It is becoming increasingly appreciated that the variation in R-R intervals can provide actionable information regarding the physiological stress and fatigue levels during and after training. A variety of mathematical and algorithmic models that represent R-R intervals can be used to present the data in time or frequency domains or even in non-linear methods. Despite the complexity of the mathematics involved in these methods, wrist watch monitors such as those made by Polar or Suunto or portable devices made by Omegawave Sport Technology Systems can collect the data for additional analysis using widely available software. As an example, autonomic activation may be evaluated by analyzing the HRV to estimate the sympathetic-vagal balance (41,49). The frequency-domain analysis of HRV provides different parameters related to sympathetic activity (low frequency/LF) or parasympathetic (vagal) activity (high frequency/HF). Both LF and HF may be given as absolute values or ratios (LF/HF). Additionally, low frequency and high frequency parameters of HRV may be provided as normalized values (LFn and HFn) by calculating the fraction of LF or HF relative to the total minus very low frequency (VLF) (13). The standard deviation of the N- N intervals (SDNN) has also been associated with changes in vagal activity (31). 2.2. Measurement of HRV during Different Exercise Intensities The sympathovagal balance changes in response to different intensities and durations of aerobic training, as evidenced by changes in HRV measures, including significant changes LF, HF, and total power of the frequency domain. In studies of a recreational cyclist, changes in the HRV power spectra were detected in an intensity-dependent manner (21) (Figure 4). Challenged with a workload of 60 W that was increased by 20 W every 3 min, the HRV power spectra of a cyclist differed quantitatively before and after a series of 20-min exercise pulses at various workloads. At baseline, the normalized LF (LFn) was slightly greater than the normalized HF (HFn). As exercise intensity increased over time, the LF/HF ratio increased with exercise intensity, reflecting an increase in the sympathetic tone (increased LFnu) and a decrease in the parasympathetic tone (decreased HFnu). 111 Figure 4. HRV Power Spectra of Recreational Athlete Before and After a Series of 20-min Exercise Impulses at Various Workloads. Vertical axis represents power spectrum density while horizontal axis depicts frequency of each frequency band. Circles describe relationship between Low Frequency (LFn) and High Frequency (HFn) bands in normalized units during rest and different intensity of exercise. The area under three different lines represent area of Total Power (TP) during rest (solid line) and different exercise intensity (dotted lines). A: before exercise; B: at 50% dVO /dt max, HR 125 beats·min-1, lactate 1.7 mmol·L-1; C: at 80% 2 dVO /dt max, HR 155 beats·min-1, lactate 3.0 mmol·L-1). Used with permission and translated from Hottenrott 2 et al. (21). The results of HRV spectra indicated by LFn and HFn in exercise vary between different reports. For example, a study of the differences in HRV at different ventilatory thresholds (VTs) identified a sympathetic predominance (indicated by an increased LF/HF ratio) during relatively less intense exercise and parasympathetic predominance (indicated by a decreased LF/HF ratio) during relatively more intense exercise. Cottin et al. (14) investigated 11 regional elite triathletes (age, 14.6 ± 1.1 yrs) who were challenged with a moderate-intensity test (below VT power) or high-intensity test (above VT power) until exhaustion. Under each circumstance, the R-R interval, VO , VCO , and blood lactate 2 2 levels were measure. They identified higher absolute LF, HF, and TP values at moderate-intensity compared to high-intensity cycling. The normalized results indicated that the LFn was significantly higher in cycling below VT (LF 80% ± 10% vs. HF 20% ± 10%, P<0.001), indicating predominance of the sympathetic input (14). The opposite was seen during heavy exercise (LF 11% ± 8% vs. HF 89% ± 8%, P<0.001), which indicated predominance of the parasympathetic input (14). These results may be explained by changes in the breathing rate combined with disappearance of the cardiac autonomic control that occurs with heavy exercise conditions. Furthermore, the LF/HF ratio was always >1 for cycling below VT and <1 for cycling above VT (4.92 ± 2.4 and 0.14 ± 0.12, respectively; P<0.001) (14). This gradual switch of the LF/HF ratio implies the overstepping of the VT and could be a reliable index of VT detection from the HRV. Although Cottin and colleagues (14) found an HFn predominance only under conditions of high- intensity exercise, Pichon et al. (34) reported different patterns in the HFn and LFn distribution as 112 physical effort increased. Fourteen healthy-trained subjects exercised for 3, 6, and 9 min at 60% and 70% of the power achieved at PVO max and for 3 and 6 min (or 3 min twice) at 80% PVO max 2 2 (power achieved at maximal oxygen consumption). With increasing exercise intensity, the HFn component reflecting parasympathetic modulation increased, whereas the LFn component reflecting sympathetic modulation decreased. The authors concluded that parasympathetic respiratory control and nonautonomic mechanisms may influence the HF-peak shift with strenuous exercise, whereas the indices of sympathetic activity do not reflect changes in autonomic modulation with exhaustive exercise (34). The HRV indices change with exercise, reflecting the changes in the autonomic system that occurs (summarized in Table 1). Recent studies illustrate that exercise and increasing exercise intensities results in detectable changes in HRV measures, reflecting the relative input of the autonomic system the body makes in response. Table 1. Measurement of HRV during Different Exercise Intensities. Publication Subjects Test HRV Other Results (n) Protocol Variables Variables Hottenrott et 1 Bicycle HFnu, LFnu VO max, Changes in the power 2 al., 2006 ergometer lactate, spectra of HRV were (21) recreational HR identified with Increased cyclist cycling intensity (50% VO 2 (male) max and 80% VO max). 2 Increased LFnu was identified with increased cycling intensity. Cottin et al., 11 Bicycle TP, LF, HF, VO ,VCO2,V At moderate intensity, 2 2004 ergometer LFnu, HFnu, E, VT, lactate cycling (30% below PVT) (14) regional LF/HF, RR compared to high intensity (Enry, cycling (10% above PVT) Cedex, higher values of HF, LF and France) TP was identified. Higher elite LFnu was seen with triathletes moderate intensity cycling, (9 males, whereas higher HFnu was 2 females) found at high intensity cycling. LF/HF was always >1 during moderate intensity cycling, whereas during high intensity cycling LF/HF was <1. Pichon et al. 14 Bicycle ergometer LF, HF, LFnu, %PVO max With increased exercise 2 2004 healthy HFnu, LF/HF intensity, increased HFnu (34) trained and lower LFnu was subjects identified. Increasing (male) exercise intensity was associated with shift HF peak frequency related to an increase in respiratory rate. LF Low frequency power spectra; HF High frequency power spectra; LFnu Normalized units of low frequency power; HFnu Normalized units of high frequency power; TP Total power of HRV power spectra; LF/HF low frequency power spectra to high frequency power spectra ratio; HR Heart rate; VO2 max Maximal oxygen consumption; VO2 Oxygen consumption (absolute in L·min-1); VCO2 Carbon dioxide release (absolute in L·min-1); VT Ventilatory threshold; %PVO2 max Percentage of cycling power output achieved at maximal oxygen consumption.

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Tommy Boone, PhD, MBA . a small portable device capable of obtaining long-term ambulatory ECGs (>24 hr) . sports medicine databases (PubMed, MEDLINE, NSCA, and ACSM) were the recovery of the body is sufficient (24).
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